The impact of embolization endpoints on the efficacy of uterine artery embolization for adenomyosis

Background This study aimed to assess how embolization endpoints affect the efficacy of uterine artery embolization (UAE) for adenomyosis.

In this single-center retrospective cohort study, patients treated with UAE from 2014–2018 received the standard embolization endpoint (SEE), while those from 2019–2022 received the delayed embolization endpoint (DEE). Clinical outcomes, including embolic microsphere volume, uterine volume, CA125 levels, hemoglobin, menstrual flow, dysmenorrhea, and postoperative complications, were compared between the groups.

At six months post-procedure, all patients showed significant improvement in clinical indicators (p < 0.01). Group DEE used significantly more embolic microspheres than Group SEE (p < 0.01) and achieved greater reductions in CA125, menstrual volume, and dysmenorrhea (p 0.05).

UAE is a safe and effective treatment for adenomyosis. Compared to the standard approach, the delayed embolization endpoint provides superior symptom relief and warrants broader clinical adoption.

Adenomyosis (AM) is a common benign gynecological disease, that mainly affects women aged 30 to 50 years. The main symptoms of adenomyosis include dysmenorrhea, menorrhagia, infertility, and an enlarged uterus [Citation1–6]. Adenomyosis affects approximately 20% of women of reproductive age globally [Citation7]. In recent years, the incidence of AM has been increasing yearly, and the age of onset has become younger, which has seriously endangered the health of women. Total hysterectomy remains the only curative option at present. However, a study suggests that there appears to be no significant difference in efficacy and quality of life between total hysterectomy and subtotal hysterectomy [Citation8]. Furthermore, robot-assisted lesion resection seems to result in less trauma and greater patient benefits [Citation9]. With the continuous advancement of medical treatment devices, non-invasive treatment technologies are gaining increasing attention. Examples include high-intensity focused ultrasound (HIFU), percutaneous microwave ablation (PMWA), and radiofrequency ablation (RFA) [Citation10]. Due to their advantages of low invasiveness, reliable efficacy, and cost-effectiveness, these treatments have been rapidly adopted in clinical practice. Uterine artery embolization (UAE) has the advantages of less trauma, uterine preservation, and quick Post-procedure recovery, and has been widely used in the clinical treatment of adenomyosis [Citation11]. Whether the artery can be completely embolized determines the curative effect of UAE [Citation4]. International studies on the effects of different embolism endpoints on efficacy and complications are limited. The purpose of this study was to retrospectively analyze and compare the impact of embolization endpoints on the efficacy of uterine artery embolization for adenomyosis.

Clinical data From September 2014 to January 2022, 323 patients with adenomyosis were treated in our center, and 78 patients met all inclusion criteria, did not meet any exclusion criteria, and completed follow-up. Adenomyosis was diagnosed through magnetic resonance imaging (MRI) examination, laboratory examination and clinical symptoms, and was not complicated by other uterine diseases. From 2014 to 2018, 36 patients with adenomyosis who underwent UAE treatment at our center were classified as the standard embolization endpoint group (Group SEE), while 42 patients treated from 2019 to 2022 were classified as the delayed embolization endpoint group (Group DEE). There was no statistically significant difference in the general data of the two groups of patients (p > 0.05) (). This study was a retrospective study and did not require ethics committee approval. All patients signed a written consent form prior to the intervention, acknowledging that medical samples might be used for current or future medical research. During the follow-up process, patients were clearly and thoroughly informed about the content and purpose of the study, and verbal consent was obtained again. Inclusion and exclusion criteria The inclusion criteria were as follows: Adenomyosis confirmed by clinical symptoms, gynecological examination, combined with Cancer Antigen 125 (CA125) laboratory test, imaging diagnosis; Patients subjectively accepted interventional embolization and understood its possible complications. Exclusion criteria were: Pregnancy; Any other possible gynecological comorbidities, such as uterine fibroids, endometriosis, etc.; Malignant tumors; Contraindications to uterine artery embolization, such as coagulation disorder; Allergy to contrast media and anesthetics; Dysfunction of important organs such as the heart, liver, lungs, and kidneys; Had received or currently undergoing treatment for adenomyosis, such as hormone therapy, surgical treatment, etc. Procedures Embolization is performed after embolic microspheres are mixed with a contrast agent into a suspension. Standard Embolization Endpoint: continue injecting until the suspension remains in the main uterine artery for five cardiac cycles; Delayed Embolization Endpoint: continue injecting until the suspension remains in the main uterine artery for at least one minute (reimage at one minute of waiting) (, black arrow). The operation time of UAE is selected within 3–7 days after menstruation is complete. Procedure steps: the patient is placed in the supine position, the right femoral artery is punctured with the modified Seldinger method, a 4-5 F vascular sheath (Terumo Corporation, Tokyo, Japan) is placed, and the pigtail catheter is inserted into the lower abdominal aorta and an aortogram is performed to delineate the anatomy of the uterine arteries. A 4-5 F RUC catheter (Merit Medical System Inc, South Jordan, USA) was used along the Roadmap to select uterine arteries by using a 2.7 F microcatheter (Progreat Micro Catheter System, Terumo Corporation, Japan), and a suspension of 300-500 μm Embospheres microspheres (Merit Medical System Inc, UT, USA) mixed with a contrast agent was administered via the microcatheter for embolization. Patients were divided into Standard Embolization Endpoint group (Group SEE) and Delayed Embolization Endpoint group (Group DEE) according to the embolization endpoint. After bilateral uterine artery embolization, aortic angiography at the level of the renal arteries was performed. If the angiogram revealed adenomyosis lesions supplied by ovarian arteries, embolization of the ovarian arteries was performed, and the endpoint of embolization was the same as above. The puncture point of the femoral artery was bandaged with pressure and immobilized for six to eight hours, with continuous electrocardiogram (ECG) monitoring during the period. Observation indicators Six months after the operation, the two groups were followed up to observe the changes in uterine volume, serum CA125 levels, hemoglobin levels, menstrual volume, dysmenorrhea pain level, and postoperative complications. The uterine volume was calculated using the formula AP*LR*CC*0.5236; Serum CA125 carbohydrate antigen was detected by the electrochemiluminescence method; Hemoglobin was detected by a colorimetric method; Menstrual flow was calculated using a pictorial blood loss assessment chart (PBAC) scoring scale; The degree of dysmenorrhea was evaluated by the Visual Analog Scale (VAS), and the patients performed a self-evaluation according to the actual situation. Statistical analysis Statistical analysis of the data was performed using SPSS 26.0 statistical software (IBM Corp., Armonk, NY, USA). The measurement data are expressed herein as the mean ± standard deviation(), and the data conforming to the normal distribution and homogeneity of variance were tested by the t-test; the data not conforming to the normal distribution were tested by the rank sum test. The count data are expressed as rates (%), and the χ2 test was used. p < 0.05 indicates that the difference is statistically significant (*: p < 0.05; **: p < 0.01; ***: p < 0.001).

Intra-group comparison In order to minimize the impact of recall bias on this retrospective study, the follow-up period was six months. Six months after UAE, according to the follow-up results, the postoperative indicators of the SEE group were compared with those before UAE. The uterine volume (284.77 vs. 130.68, p < 0.01) (cm3), serum CA125 level (163.70 vs. 23.35, p < 0.01) (U/ml), and hemoglobin level (111.44 vs. 128.28, p < 0.01) (g/L), menstrual volume (321.50 vs. 60.00, p < 0.01) and degree of dysmenorrhea (9.00 vs. 1.50, p < 0.01) were significantly improved compared with those before surgery (). The postoperative indicators of the DEE group were compared with those before UAE. The uterine volume (233.05 vs. 143.35, p < 0.01) (cm3), serum CA125 level (160.25 vs. 40.76, p < 0.01) (U/ml), and hemoglobin level (114.50 vs. 129.00, p < 0.01) (g/L), menstrual volume (335.50 vs. 26.00, p < 0.01) and degree of dysmenorrhea (10.00 vs. 0.00, p < 0.01) were also significantly improved compared with those before UAE (). Comparison between groups The comparison method between groups adopts the difference comparison method: changes in the difference between preoperative and postoperative uterine volumes in Groups SEE and DEE (preoperative uterine volume - postoperative uterine volume); the difference between preoperative and postoperative serum CA125 values between Group SEE and DEE (preoperative serum CA125 value - postoperative serum CA125 value); Group SEE and DEE preoperative and postoperative hemoglobin numerical difference change (postoperative hemoglobin value - preoperative hemoglobin value); Group SEE and DEE before and after operation menstrual flow difference change (preoperative menstrual flow - postoperative menstrual flow); Group SEE and DEE before operation changes in difference with postoperative dysmenorrhea score (preoperative dysmenorrhea score - postoperative dysmenorrhea score). The complications were divided into minor, moderate and severe complications, and the incidence rates were compared [Citation12]. The volume of embolic microspheres used in Group DEE was significantly higher than that in Group SEE (9.50 vs. 6.50, p < 0.01), and the improvement of serum CA125 level(110.96 vs. 59.05)(U/ml), menstrual volume(315.43 vs. 212.97), and dysmenorrhea level(8.00 vs. 5.50)in Group DEE were better than those in Group SEE, and the difference was statistically significant (p < 0.05) () () (); There was no statistical difference between the SEE group and the DEE group in postoperative uterine volume improvement (143.00 vs. 100.25, p = 0.107) (cm3) and hemoglobin improvement (16.83 vs. 13.17, p = 0.248) (g/L) (). There was no statistically significant difference in the incidence of postoperative complications between the SEE group and the DEE group (p > 0.05) () ().

AM is a common benign diseases in gynecology in which endometrial epithelial cells and stromal fibroblasts are extended or surrounded by hypertrophic smooth muscle cells ectopically in the myometrium [Citation5,Citation13]. Due to its unique pathological process, the boundary between lesion tissue and normal tissue is often unclear. Surgical excision of lesions is generally considered incapable of completely removing the lesion tissue, and the risk of uterine rupture increases significantly after surgical treatment for adenomyosis [Citation14]. The same challenge exists with HIFU and ablation therapies. However, the differing blood supply characteristics between lesion tissue and normal tissue naturally serve as their boundary. Because AM lesions have poor tolerance to ischemia and hypoxia, while normal uterine tissue has a rich vascular communication network and is more tolerant to ischemia and hypoxia, the blood supply of the lesion is blocked by embolization of bilateral uterine arteries. This leads to ischemic necrosis of the lesion, followed by dissolution and absorption, to achieve the purpose of relieving symptoms [Citation15]. The delayed embolization endpoint adopted in this study can block the blood flow of AM lesions to the greatest extent, and the clinical symptoms have been significantly improved under the condition that the safety is similar to that of the standard embolization endpoint. The blood supply arterial network of the AM can be divided into inner and outer layers. The outer layer of the vascular network mainly exists in the myometrium and the surface of the lesion. The outer layer of the vascular network is small and has no thick vascular network frame. Inside the myometrial lesions, the inner capillary network is small, dense, and diffusely distributed, which is the neovascularization of the lesion ( Blue Arrow) [Citation15]. In the treatment of AM in UAE, the distribution of embolic agents in the lesions mainly depends on the abundance of blood vessels in the lesions. Compared with uterine fibroids, in AM, embolic agents mainly accumulate in the lesions and the myometrium after arterial embolization, and AM does not have the typical outer vascular network of arteries feeding uterine fibroids (, white arrow). The presumed reasons are as follows: Compared with fibroid lesions, adenomyosis usually has a poorer blood supply; Adenomyosis lesions are often ill-defined and irregular, and the progression of endometrial cells and focal angiogenesis is similar to that of tumor metastasis. Additionally, adenomyotic lesions do not have a fibroid-like pseudocapsule, and the outer vascular network is sparse, the main blood supply comes from the small and slow-flowing internal vascular network [Citation16]. The above arguments lead to a reduced efficiency of embolic agent entry into the lesion, however, studies have shown that the necrotic cross-sectional area of adenomyosis after UAE should reach at least 34.3% to reduce the possibility of recurrence [Citation17], which further emphasizes the importance of complete embolization. In order to further improve the degree of embolization of UAE in the treatment of adenomyosis, Kim et al. [Citation18] proposed that the use of polyvinyl alcohol (PVA) particles of smaller size (250 ∼ 355 μm) will significantly increase the necrosis rate of adenomyosis, compared with the use of 355 μm∼500μm PVA particles. The same group, Kim et al. [Citation19], also proposed to use 150 ∼ 250μm PVA particles first, and then use 250 ∼ 355μm and 355 ∼ 500μm PVA particles (called the 1-2-3 plan) in order to improve the degree of embolization. They believed that it could increase the necrosis rate of adenomyosis. Existing studies achieve more complete embolization by using smaller-sized embolization particles, while this study improves the degree of embolization by prolonging the embolization end point. During the UAE operation, the blood flow of the main uterine artery gradually slows down, and the blood flow to the lesion gradually decreases. In view of the small capillary network inside the lesion, the blood flow itself is relatively slow. In addition, after the injection of embolic agents, the blood flow of the main uterine artery decreases, the force of blood flow to the internal vascular network decreases, and the resistance increases, resulting in a longer time for the embolic agent to flow to the internal capillary network of the lesion. Conjecturing standard embolic endpoints only keeps embolic agents proximal to the vascular network, but cannot completely block the blood flow. With a longer embolization endpoint, the embolic agent has sufficient time to be pushed into small blood vessels with the blood flow, further aggravating tissue ischemia and hypoxia, and reducing the generation of collateral supply vessels to achieve necrosis. Thanks to the strong sensitivity and specificity of MRI in diagnosing adenomyosis [Citation20,Citation21], patients who undergo delayed embolization endpoint show no enhancement of the lesions on imaging after surgery, the endometrial tissue and glands that invaded the myometrium may have undergone more complete stromal degeneration and necrosis. During menstruation, the number of abnormal endometrial glands stripped from the myometrium is lower, so the reduction of menstrual flow and the relief of dysmenorrhea are significantly better than those of patients with standard embolization endpoints. The greater reduction in tumor-like lesions with the use of delayed embolization endpoint also results in a more significant decrease in serum CA125. Since UAE was first proposed and has been in clinical application for more than 20 years, its effectiveness and safety in the treatment of symptomatic uterine fibroids and adenomyosis have been widely verified [Citation2,Citation22,Citation23]. Most scholars believe that uterine-ovarian artery anastomosis leads to lesion reperfusion as a potential cause of failure after UAE treatment [Citation24,Citation25]. We unexpectedly found that delayed embolization endpoints can be used to perform reliable retrograde embolization of the ovarian artery via the utero-ovarian artery communicating branch (, white arrow). AM lesions have multiple blood vessels, mainly supplied by bilateral uterine arteries, and in a few patients, spiral descending ovarian arteries can be seen. As early as 1980, Karlsson et al. stated that the anastomotic branch of the uterine-ovarian artery exists in all women. When the patient has uterine or ovarian abnormalities, the anastomotic port diameter is increased to supplement the blood supply [Citation26,Citation27]. This study is also consistent with the pathological development of AM, confirming that embolic agents can retrogradely embolize the ovarian artery through this anastomotic branch. Some scholars expressed concerns about the impact of UAE on ovarian function. Embolization agents embolize the ovarian artery through the utero-ovarian artery communicating branch, causing hypoxic damage to ovarian tissue and amenorrhea, leading to premature ovarian failure [Citation28]. However, several studies have shown that ovarian artery embolization does not have a strong correlation with the impact on ovarian function. An analysis (n = 353) including three cohort studies and three case-control studies showed that there was no significant change in serum anti-Mülllerian hormone (AMH) and serum follicle-stimulating hormone (FSH) levels after UAE [Citation7]. Kim et al. performed UAE using embolic microspheres. Postoperative histological examination found the presence of embolic microspheres in the adnexa, and all subjects had viable ovaries and fallopian tubes without evidence of focal ischemia or infarction [Citation29]. From the above studies, it is speculated that recent data tend to show no significant change in ovarian function between the preoperative and postoperative UAE status, which further proves the necessity of ovarian artery embolization. In the actual interventional protocol of our center, when AM patients underwent delayed embolization, retrograde embolization of the ovarian artery by embolization microspheres was seen in the later stage of embolization, Postoperative angiography proved that the blood flow supplied by the ovarian artery to the lesion could be blocked, resulting in a more effective and thorough embolization (, white arrow). However, the standard embolization endpoint is not as good as the delayed embolization endpoint because the ovarian artery continues to supply AM lesions due to insufficient embolization time in the later stage. Embolization can also be performed by additional cannulation through the abdominal aorta to the ovarian artery; however, it is difficult to clearly display the ovarian artery both in preoperative magnetic resonance angiography (MRA) examination and intraoperative angiography, and the difficulty of selection leads to the preservation of the blood supply of the lesion, prolonging the operation time, increasing the exposure dose, and increasing the risk of nontarget embolism. During the postoperative follow-up of the patients with the two embolism endpoints, some patients reported that there were no menstrual cramps or oligomenorrhea within three months after the operation, but almost all patients indicated that menstruation returned to normal during the three-month follow-up, consistent with recent literature reports. One case of postoperative menopause occurred in Group SEE; this patient was 48 years old when she was admitted to the hospital, and the average age of menopause in Chinese women is 48.7 (4.3) years [Citation30]. The patient’s AMH levels decreased before the operation, and there was a possibility of ovarian failure. It was concluded that the patient was physiologically menopausal rather than having surgery-related complications. There was one case of nontargeted embolism in Group DEE, which accidentally embolized the inferior gluteal artery; the patient was discharged after being cured in the hospital.

This study is a retrospective study. There was a high possibility of recall bias, the sample size was limited, and there was no histopathological confirmation after surgery. Consequently, the present findings need to be further verified by prospective clinical trials with large samples. At the same time, because there is still controversy internationally on whether patients with adenomyosis with ovarian artery collateral supply should undergo ovarian artery embolization, the safety of retrograde embolization of the ovarian artery mentioned in this article can only be confirmed within the follow-up time interval of this study, and still needs to be confirmed by studies with large samples and long-term follow-up.

Uterine artery embolization in the treatment of AM with a delayed embolization endpoint can embolize the artery supplying the lesion more effectively and enhance the curative effect compared with that involving use of the standard embolization endpoint, and there was no significant difference in safety during the follow-up period of this study. Ethical approval This study has been approved by The Ethics Committee of The Second Affiliated Hospital of Soochow University, decision number: JD-HG-2025-047. Disclosure statement No potential conflict of interest was reported by the author(s). Data availability statement The datasets generated and/or analysed during the current study are not publicly available due to patient privacy protection requirements, but are available from the corresponding author upon reasonable request. Additional information Funding

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